Helicase-DNA polymerase interaction is critical to initiate leading-strand DNA synthesis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 23, 2011, Pages 9372-9377

  Zhang, Huidong ^a   Lee, Seung Joo ^a   Zhu, Bin ^a   Tran, Ngoc Q ^a   Tabor, Stanley ^a   Richardson, Charles C ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

DNA polymerase helicase interaction; Strand displacement DNA synthesis; T7 bacteriophage; T7 replisome

Indexed keywords

ASPARAGINE; DNA POLYMERASE; DOUBLE STRANDED DNA; GENE 4 HELICASE; GENE 5 DNA POLYMERASE; HELICASE; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIOPHAGE T7; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; DNA BINDING; DNA REPLICATION; DNA SYNTHESIS; GENE INTERACTION; PRIORITY JOURNAL; PROTEIN INTERACTION;

BACTERIOPHAGE T7; BINDING SITES; DNA HELICASES; DNA REPLICATION; DNA, SINGLE-STRANDED; DNA, VIRAL; DNA-DIRECTED DNA POLYMERASE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SURFACE PLASMON RESONANCE; THIOREDOXINS; VIRAL PROTEINS;

EID: 79959357956     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1106678108     Document Type: Article

References (29)

1. Hamdan SM, Richardson CC (2009) Motors, switches, and contacts in the replisome. Annu Rev Biochem 78:205-243.
2. Tabor S, Huber HE, Richardson CC (1987) Escherichia coli thioredoxin confers processivity on the DNA polymerase activity of the gene 5 protein of bacteriophage T7. J Biol Chem 262:16212-16223.
3. Marintcheva B, Hamdan SM, Lee SJ, Richardson CC (2006) Essential residues in the C terminus of the bacteriophage T7 gene 2.5 single-stranded DNA-binding protein. J Biol Chem 281:25831-25840. (Pubitemid 44401971)
4. Johnson A, O'Donnell M (2005) Cellular DNA replicases: Components and dynamics at the replication fork. Annu Rev Biochem 74:283-315. (Pubitemid 40995509)
5. Benkovic SJ, Valentine AM, Salinas F (2001) Replisome-mediated DNA replication. Annu Rev Biochem 70:181-208. (Pubitemid 32662209)
6. Hamdan SM, et al. (2005) A unique loop in T7 DNA polymerase mediates the binding of helicase-primase, DNA binding protein, and processivity factor. Proc Natl Acad Sci USA 102:5096-5101.
7. Ghosh S, Marintcheva B, Takahashi M, Richardson CC (2009) C-terminal phenylalanine of bacteriophage T7 single-stranded DNA-binding protein is essential for strand-displacement synthesis by T7 DNA polymerase at a nick in DNA. J Biol Chem 284:30339-30349.
8. Lee JB, et al. (2006) DNA primase acts as a molecular brake in DNA replication. Nature 439:621-624.
9. Jeong YJ, Levin MK, Patel SS (2004) The DNA-unwinding mechanism of the ring helicase of bacteriophage T7. Proc Natl Acad Sci USA 101:7264-7269. (Pubitemid 38638021)
10. Stano NM, et al. (2005) DNA synthesis provides the driving force to accelerate DNA unwinding by a helicase. Nature 435:370-373. (Pubitemid 40745548)
11. Doublie S, Tabor S, Long AM, Richardson CC, Ellenberger T (1998) Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 angstrom resolution. Nature 391:251-258.
12. Hamdan SM, et al. (2007) Dynamic DNA helicase-DNA polymerase interactions assure processive replication fork movement. Mol Cell 27:539-549. (Pubitemid 47238626)
13. Loparo JL, Kulczyk AW, Richardson CC, van Oijen AM (2011) Observing polymerase exchange by simultaneous measurements of replisome composition and function at the single-molecule level. Proc Natl Acad Sci USA 108:3584-3589.
14. Yang J, Zhuang Z, Roccasecca RM, Trakselis MA, Benkovic SJ (2004) The dynamic processivity of the T4 DNA polymerase during replication. Proc Natl Acad Sci USA 101:8289-8294. (Pubitemid 38736568)
15. Brieba LG, et al. (2004) Structural basis for the dual coding potential of 8-oxoguanosine by a high-fidelity DNA polymerase. EMBO J 23:3452-3461. (Pubitemid 39265535)
16. Lee SJ, Chowdhury K, Tabor S, Richardson CC (2009) Rescue of bacteriophage T7 DNA polymerase of low processivity by suppressor mutations affecting gene 3 endonuclease. J Virol 83:8418-8427.
17. Notarnicola SM, Mulcahy HL, Lee J, Richardson CC (1997) The acidic carboxyl terminus of the bacteriophage T7 gene 4 helicase/primase interacts with T7 DNA polymerase. J Biol Chem 272:18425-18433. (Pubitemid 27306437)
18. Lee SJ, Marintcheva B, Hamdan SM, Richardson CC (2006) The C-terminal residues of bacteriophage T7 gene 4 helicase-primase coordinate helicase and DNA polymerase activities. J Biol Chem 281:25841-25849. (Pubitemid 44401972)
19. Singleton MR, Sawaya MR, Ellenberger T, Wigley DB (2000) Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides. Cell 101:589-600.
20. Johnson DE, Takahashi M, Hamdan SM, Lee SJ, Richardson CC (2007) Exchange of DNA polymerases at the replication fork of bacteriophage T7. Proc Natl Acad Sci USA 104:5312-5317. (Pubitemid 47175677)
21. Tabor S, Richardson CC (1995) A single residue in DNA polymerases of the Escherichia coliDNA polymerase I family is critical for distinguishing between deoxyribonucleotides and dideoxyribonucleotides. Proc Natl Acad Sci USA 92:6339-6343.
22. Kim DE, Narayan W, Patel SS (2002) T7 DNA helicase: A molecular motor that processively and unidirectionally translocates along single-stranded DNA. J Mol Biol 321:807-819.
23. Patel SS,Wong I, Johnson KA (1991) Pre-steady-state kinetic analysis of processive DNA replication including complete characterization of an exonuclease-deficient mutant. Biochemistry 30:511-525.
24. O'Donnell M (2006) Replisome architecture and dynamics in Escherichia coli. J Biol Chem 281:10653-10656.
25. Perumal SK, Yue H, Hu Z, Spiering MM, Benkovic SJ (2010) Single-molecule studies of DNA replisome function. Biochim Biophys Acta 1804:1094-1112.
26. Weigel C, Seitz H (2006) Bacteriophage replication modules. FEMS Microbiol Rev 30:321-381.
27. Crampton DJ, Ohi M, Qimron U, Walz T, Richardson CC (2006) Oligomeric states of bacteriophage T7 gene 4 primase/helicase. J Mol Biol 360:667-677. (Pubitemid 43975114)
28. McInerney P, Johnson A, Katz F, O'Donnell M (2007) Characterization of a triple DNA polymerase replisome. Mol Cell 27:527-538. (Pubitemid 47238627)
29. Indiani C, McInerney P, Georgescu R, Goodman MF, O'DonnellM(2005) A sliding-clamp toolbelt binds high-and low-fidelity DNA polymerases simultaneously. Mol Cell 19:805-815. (Pubitemid 41316674)